Influence of larval density and dietary nutrient

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concentration, higher larval density resulted in higher individual larval weight and total larval yield, ... seems that availability of balanced amounts of calories, fat,.
DOI: 10.1111/eea.12716

Influence of larval density and dietary nutrient concentration on performance, body protein, and fat contents of black soldier fly larvae (Hermetia illucens) Karol B. Barragan-Fonseca1,2*, Marcel Dicke1

& Joop J.A. van Loon1

1

Laboratory of Entomology, Wageningen University, PO Box 16, 6700 AA Wageningen, The Netherlands, and Departamento de Produccion Animal, Facultad de Medicina Veterinaria y de Zootecnia, Universidad Nacional de Colombia, Bogota, Colombia

2

Accepted: 27 June 2018

Key words: detritivory, diet quality, growth, nutritional value, ration, survival, Diptera, Stratiomyidae

Abstract

Performance and body composition of insect larvae depend on quality and quantity of their diet, and on biotic factors such as larval density. We investigated the effect of dietary nutrient concentration and larval rearing density on survival, development, growth, and protein and fat contents of larvae of the black soldier fly (BSF), Hermetia illucens L. (Diptera: Stratiomyidae). Neonate larvae were fed with a low (NC1), intermediate (NC2), or high nutrient concentration (NC3), and with four rearing densities (50, 100, 200, or 400 larvae per container). Two feeding regimes (FR) were tested: in FR1, the amount of diet added during the experiment was based on the visually estimated larval mass present, whereas in FR2, a fixed feeding ration of 0.6 g of food per larva was applied at the start. FR1 resulted in food limitation, resulting in significantly lower body crude protein content on diet NC1 than on NC2 at larval densities 100 and 200. Larval crude fat content was higher on diets with higher nutrient concentration and at lower larval densities. For FR2, development time was shorter on diets with higher nutrient concentration and at lower larval densities. Individual larval weight and total larval yield increased with higher nutrient concentration at all four larval densities. At lower nutrient concentration, higher larval density resulted in higher individual larval weight and total larval yield, revealing an interaction between larval density and dietary quality. Larval crude protein content was higher at lower densities and lower nutrient concentration. Larval crude fat was higher at higher larval densities and nutrient concentrations. This study indicates that larval protein content is regulated within narrow limits, whereas larval crude fat content is strongly affected by nutrient concentration and by larval density.

Introduction The size to which an individual insect grows is affected by both genetic and environmental factors that operate through complex molecular and physiological mechanisms (Nijhout, 2003). Growth rate varies substantially in response to various stimuli, including resource availability, competition, predator presence, time of season, humidity, and temperature (Scriber & Slansky, 1981; Harnden & Tomberlin, 2016). Moreover, food quality affects many *Correspondence: Karol B. Barragan-Fonseca, Departamento de Producci on Animal, Facultad de Medicina Veterinaria y de Zootecnia, Universidad Nacional de Colombia, Bogota, Colombia. E-mail: [email protected]

life-history traits such as larval and adult performance (Moreau et al., 2006). High food quality enhances the rate of development and increases survival in some insect species (de Haas et al., 2006). For example, Nguyen et al. (2013) and Oonincx et al. (2015b) observed that the detritivorous larvae of the black soldier fly (BSF), Hermetia illucens L. (Diptera: Stratiomyidae), when fed diets of vegetable by-products high in protein, had a shorter development time (21 days) than larvae fed low-protein diets (37 days). Conversely, Simon et al. (2011) suggested that diets with a higher proportion of protein increase development time and survival rate of some predatory fly species. Nguyen et al. (2013) established an increase in growth rate and decrease in developmental duration of BSF larvae

© 2018 The Authors. Entomologia Experimentalis et Applicata published by John Wiley & Sons Ltd on behalf of Netherlands Entomological Society Entomologia Experimentalis et Applicata 166: 761–770, 2018 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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on both high-protein and high-fat diets. However, indications have been found that high levels of fat – 20–36% crude fat based on dry matter (DM) – may be detrimental for both larval and adult survival, lifespan, and reproductive output (Ujvari et al., 2009; Nguyen et al., 2013). It seems that availability of balanced amounts of calories, fat, and protein may be more important for fast development and higher larval weight than only a high-protein content (Nguyen et al., 2013). Although BSF larvae on average contain both a highprotein and a high-fat level compared to other edible insect species (Zheng et al., 2012a; Barragan-Fonseca et al., 2017), body composition of the larvae depends on the quality and quantity of ingested food (Nguyen et al., 2015; Oonincx et al., 2015a,b). Consequently, larvae fed on different substrates had varying body protein (ranging from 37.0 to 62.7% DM) and fat content (6.6–39.2% DM) (Barragan-Fonseca et al., 2017). Also physical factors may influence insect performance. For example, if the layer of food substrate consisting of meat meal, swine meat, fish, or liver is too thick, larval food intake is reduced resulting in lower survival and longer developmental time (Nguyen et al., 2013). Larde (1989) fed BSF larvae on coffee-pulp substrates with different composition, and observed that BSF larvae grow better on the most homogeneous, dense, and dry substrate (780 g kg 1 wet matter solids). Moisture levels of 60–70% in manure and chicken feed have been found adequate for BSF larvae (Fatchurochim et al., 1989; Tomberlin et al., 2002; Myers et al., 2008; Holmes, 2010). However, due to the variable composition of organic waste, food moisture is difficult to control and needs to be evaluated not only under laboratory but also under field conditions where evaporation rate fluctuates. Biotic factors may also affect BSF performance. For example, larval density can be a major factor affecting the rate of development (Tomberlin et al., 2002; Diener et al., 2009). Parra Paz et al. (2015) demonstrated that larval density has a significant influence on bioconversion of residual organic matter into body mass by BSF. BSF larvae tend to aggregate and overcrowding slows larval development due to competition for feed (Rivers & Dahlem, 2013). Moreover, high larval densities may result in decreased substrate quality by accumulation of larval waste products (Green & Popa, 2012) and may generate direct energetic costs if larvae spend extra energy interacting with each other (Jannat & Roitberg, 2013). Compensatory mechanisms are activated in response to crowding and nutritional deficiencies. Insects have a tendency to prolong the larval period (Miller, 1964), or to increase either the rate of ingestion or the total amount of food ingested during larval development (Green et al.,

2003). Sullivan & Sokal (1963) proposed two basic types of responses to crowding: (1) a reduction in the number of individuals able to complete their life cycles, with the emerging adults maintaining normal body size, and (2) sustaining survival accompanied by reduction in body weight, as has been reported for the dipterans Phormia regina (Meigen) (Calliphoridae) (Green et al., 2002), Drosophila melanogaster Meigen, Drosophila simulans Sturtevant (Miller, 1964), and Aedes albopictus Skuse (Yoshioka et al., 2012). According to Sullivan & Sokal (1963), for the second type of response substantial losses in numbers will occur only at densities above which adult weight drops below a critical limit. Lower larval densities are not always better to maximise growth rate. In some insect species, larval aggregations provide adaptive benefits to individuals due to heat generation, which might enhance food assimilation (Green et al., 2002) and provide protection from low environmental temperature and possibly predators (Rivers & Dahlem, 2013). BSF larval weight gain is also affected because of their potential dependence on bacteria as food (Liu et al., 2008). Higher larval densities are associated with higher bacterial densities which might allow larvae to have better access to bacterially recycled nutrients, thereby resulting in more effective nutrient absorption. Therefore, optimising density may benefit the productivity of insect rearing. Detailed knowledge of the conditions required for optimal growth, development, and nutrient allocation of BSF is necessary for implementation of large-scale production systems (Coelho et al., 2013). The effect of nutrient density of the ingested food on development, growth, and body composition of BSF in interaction with larval density has not been investigated systematically before. The aim of the present study was to investigate the effect of dietary nutrient concentration (NC), larval rearing density, and the possible interaction between these two factors on growth characteristics and nutritional composition of BSF larvae.

Materials and methods Experimental insects

Hermetia illucens larvae were obtained from a colony maintained under constant conditions in a climate room (27  1 °C, 70% r.h., and L12:D12 photoperiod) at the Laboratory of Entomology, Wageningen University, The Netherlands. Experimental design

This study was based on a 3 9 4 factorial design with three levels of dietary nutrients (NC1-3) obtained by

Larval density and nutrition in black soldier fly 763

diluting commercial chicken feed (Opfokmeel Farmfood; AgruniekRijnvallei Voer, Wageningen, The Netherlands) with cellulose (Alphacel non-nutritive bulk; MP Biomedicals, Illkirch, France) (Table 1), and four rearing densities (D50-400) obtained by placing 50, 100, 200, and 400 larvae (